Download NPUAP White Paper on Nutrition - National Pressure Ulcer Advisory

The Role of Nutrition in Pressure Ulcer Prevention and Treatment:
National Pressure Ulcer Advisory Panel White Paper
Authors: Becky Dorner, RD, LD, Mary Ellen Posthauer, RD, CD,
and David Thomas, MD, CMD, FACP
National Pressure Ulcer Advisory Panel
Introduction
The purpose of this white paper is to review the
currently available scientific evidence related to
nutrition and hydration for pressure ulcer
prevention and treatment in adults; introduce the
nutrition recommendations from the new
National Pressure Ulcer Advisory Panel
(NPUAP)-European Pressure Ulcer Advisory
Panel (EPUAP) Guidelines for Pressure Ulcer
Treatment; and review research needs for the
future.
Overview of Pressure Ulcers: Prevalence,
Incidence, Cost and Nutrition
Estimates indicate that 1 to 3 million people in
the US develop pressure ulcers each year (1).
According to the Joint Commission, more than
2.5 million patients in United States (US) acutecare facilities suffer from pressure ulcers, and
60,000 die from pressure ulcer complications
each year (2).
The NPUAP defines prevalence as “a proportion
of persons who have a pressure ulcer at a
specific point in time” (3). Prevalence of
pressure ulcers in the US is widespread in all
settings with estimates of 10% to 18% in acute
care, 2.3% to 28% in long-term care, and 0% to
29% in home care (3). The NPUAP defines
incidence as “the number of new cases of
pressure ulcers appearing in a pressure ulcer free population over a period of time” (3).
Incidence of pressure ulcers ranges from 2.3%
to 23.9% in long-term care, 0.4% to 38% in
acute care, 0% to 17% in home care and 0% to
6% in rehabilitative care (3,4). In addition, new
information from Agency for Healthcare
Research and Quality (AHRQ) (5) indicates that
pressure ulcer-related hospitalizations increased
by an alarming 80 percent from 1993 to 2006.
Please note that the interpretation of incidence
and prevalence numbers require caution as
numbers are influenced by multiple factors
including definition and method of calculation
(3).
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Pressure ulcers can reduce overall quality of life
due to pain, treatments, and increased length of
institutional stay, and may also contribute to
premature mortality in some patients (6,7).
Therefore, any intervention that may help to
prevent pressure ulcers or to treat them once
they occur is important to reduce the cost of
pressure ulcer care and improve quality of life
for affected individuals.
The burden of having a pressure ulcer is high, in
physical, emotional and financial terms. Data
from 1999 indicates that the cost of treating
pressure ulcers may range from $5 to 8.5 billion
annually (8). Factor in 7% per year for health
care inflation, and this equates to approximately
$9.2 to 15.6 billion dollars in 2008. AHRQ
reported
that
pressure
ulcer-related
hospitalizations ranged from 13 to 14 days and
cost $16, 755 to $20,430 compared to the
average stay of 5 days and costs approximately
$10,000 (5). The Centers for Medicare/Medicaid
Services (CMS) reports the cost of treating a
pressure ulcer in acute care (as a secondary
diagnosis) is $43,180.00 per hospital stay (9,10).
Contributing cost factors include increased
length of stay due to pressure ulcer
complications such as pain, infection, high tech
support surfaces, and decreased functional
ability (11).
In addition to the financial cost of pressure
ulcers, mortality rates are disturbing. A recent
AHRQ document (5) reports 503,300 pressure
ulcer-related hospitalizations in 2006 which
included 45,500 hospital admissions in which
patients had pressure ulcers as the primary
diagnosis. Of these admissions, one in 25
admissions ended in death. Another 457,800
pressure ulcer-related hospital admissions noted
pressure ulcer as the secondary diagnosis. Of
these admissions, the death rate was one in
eight.
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The Role of Nutrition in Pressure Ulcer Prevention and Treatment:
National Pressure Ulcer Advisory Panel White Paper
Litigation adds to the burden of health care
costs. This is especially true in long-term care,
where nearly 87% of verdicts and out of court
settlements against facilities are awarded to the
plaintiffs (12). One report reviewed 54 nursing
home law suit cases from September 1999 to
April 2002 involving pressure ulcers. The
average monetary recovery was more than
$13.5 million and included awards of up to $312
million in one case, when determined by a
verdict or settlement (13). In litigation cases
related to pressure ulcers, jury awards are
highest for multiple causation factors. When
awards were related to single causes, the
highest awards were for those where inadequate
nutrition was alleged to be the cause of pressure
ulcers (12). However, it is important to note that
in the past few years a few states have passed
legislation limiting malpractice awards which
may help to control these cost burdens in the
future.
Nutrition and Pressure Ulcers
Although limited evidence-based research is
available, general consensus indicates that
nutrition is an important aspect of a
comprehensive care plan for prevention and
treatment of pressure ulcers (7,14,15), and it is
essential to address nutrition in every individual
with pressure ulcers. Adequate calories, protein,
fluids, vitamins and minerals are required by the
body for maintaining tissue integrity and
preventing tissue breakdown. A large cohort
study of 1524 residents in 95 nursing facilities
documented that pressure ulcer incidence may
be higher with increased age, frailty or severity
of illness, pressure ulcer history or significant
weight loss and eating difficulties (16,17).
Compromised nutritional status such as
unintentional weight loss, undernutrition, protein
energy malnutrition (PEM), and dehydration
deficits are known risk factors for pressure ulcer
development (1,18). Other nutrition-related risk
factors associated with increased risk of
pressure ulcers include low body mass index
(BMI), reduced food intake, and impaired ability
to eat independently (16,18,19).
The National Pressure Ulcer Long Term Care
Study (NPULS) was a retrospective cohort study
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of detailed resident characteristics, treatments,
and outcomes using a convenience sample of
nursing home residents. Participants included
2,420 adult residents of nursing facilities, with a
length of stay of 14 days or longer, who were at
risk of developing a pressure ulcer. More than
50% of residents in the study experienced
weight loss of at least 5% during the 12 week
study, and 45.6% of residents were considered
underweight (defined as a BMI of 22 or less).
The highest percentage of weight loss occurred
in the residents with a recent pressure ulcer. In
addition, residents with the lowest BMIs also had
existing pressure ulcers (20). Thomas (21) noted
that recent weight loss in older adults was a key
factor in mortality risk, and Murden and Ainslie
(22) indicated that a 10% decline in weight over
a 6 month period was a strong predictor of
mortality in this population.
Two studies
supported the theory that individuals in longterm care whose body weight declined by 5% in
30 days were at increased risk for death (23,24).
Thomas (25) described the “anorexia of aging”
including appetite decline, weight loss and,
decreased metabolic rate placing the elderly
person at risk for undernutrition.
Undernutrition has been defined as pure protein
and energy deficiency which is reversed solely
by the administration of nutrients (26). This
definition ultimately defines undernutrition by the
ability to improve nutritional status and reverse
the consequences of undernutrition.
Poor
outcomes
are
associated
with
undernutrition including the risk of morbidity and
mortality, hence the need to quickly identify and
treat undernutrition when pressure ulcers are
present. Undernutrition may also negatively
impact pressure ulcer healing. Conditions that
may lead to undernutrition include: increased
dependence on others for eating, chewing and
swallowing problems, decreased oral intake of
food and fluid, unintentional weight loss and
advanced age. Undernutrition may decrease the
body’s ability to fight infections and have a
negative impact on pressure ulcer healing.
Several other medical conditions may affect
pressure ulcer healing. PEM has been defined
as a wasting and excessive loss of lean body
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mass resulting from “too little energy being
supplied to the body tissue that can be reversed
solely by the administration of nutrients” (27).
Cachexia is another medical malady which may
affect pressure ulcer healing. “Cachexia is a
complex metabolic syndrome associated with
underlying illness and characterized by loss of
muscle with or without loss of fat mass. The
prominent clinical feature of cachexia is weight
loss in adults (corrected for fluid retention)…
Anorexia, inflammation, insulin resistance, and
increased muscle protein breakdown are
frequently associated with wasting disease.
Wasting disease is distinct from starvation, age
related loss of muscle mass, primary
depression, malabsorption and hyperthyroidism
and is associated with increased morbidity” (28).
Yet another concern is hypermetabolism, a
responsive increase in metabolic rate, which is
triggered by trauma, severe illness, infection,
pressure ulcers and other factors. The body
utilizes calories at a rapid rate, first pulling from
available glycogen stores, then from visceral
protein stores in order to provide energy needed
to keep the major organs functioning. At the
same time, cytokines, the proteins that are
liberated in tissue injury and that mediate the
body’s immune and inflammatory response,
contribute to metabolic and gastrointestinal
changes such as anorexia and malaise. The
effect of increased cytokines and Interleukin 1-6
(pro-inflammatory cytokines) on nutritional status
results in anorexia, muscle wasting, decreased
nitrogen retention, and impaired albumin
synthesis (29). Together, the above maladies
may contribute to unintended weight loss,
undernutrition and/or PEM which in turn are risk
factors for pressure ulcer development.
Recommendations for Practice
Nutritional Considerations in Pressure
Ulcer Prevention
Little specific evidence exists related to medical
nutrition therapy (MNT) for preventing pressure
ulcers. However, early nutrition screening and
assessment is essential to identify risk of
undernutrition, PEM and unintentional weight
loss which may precipitate pressure ulcer
development and delay healing. There are many
©2009 NPUAP
physical, functional and psychosocial factors
that can contribute to inadequate intake,
unintentional weight loss, undernutrition and/or
PEM, including cognitive deficits, dysphagia,
depression,
food-medication
interactions,
gastrointestinal (GI) disorders and impaired
ability to eat independently. No clear method
exists to determine when nutritional status
decline begins, especially in older people. In
spite of aggressive nutritional interventions,
some individuals are simply unable to absorb
adequate nutrients for good health.
Nutrition Screening and Assessment
The nutrition screening process can identify
individuals at nutritional risk and assist in making
referrals to the appropriate health care
professionals for further assessment. Initial
screening is completed on admission by a
qualified health care professional.
Several tools may be utilized in the nutrition
screening process. Langkamp-Henken and
colleagues (30) concluded from a crosssectional study that the Mini-Nutritional
Assessment (MNA) and MNA Screening Form
provided an advantage over using visceral
protein in screening and assessing nutritional
status (31). The Malnutrition Universal
Screening Tool (MUST) is another potential
screening tool which helps practitioners identify
risk of undernutrition (32). However, these tools
are not widely used in all practice areas.
The Braden Risk Assessment Scale: Predicting
pressure ulcer risk (33) includes a nutrition
subscale which yields additional data that can
be used in the nutrition screening and
assessment process. Individuals should be
reassessed following a change in condition, e.g.,
surgery, NPO status, intravenous fluid therapy
only, etc.
Based on the results of the nutrition screening, a
referral is made for a formal assessment by a
registered dietitian (RD), who then completes a
thorough nutritional assessment on each
individual
and
makes
appropriate
recommendations
for
interventions
and
management.
The
American
Dietetic
Association (ADA) Nutrition Care Process
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The Role of Nutrition in Pressure Ulcer Prevention and Treatment:
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includes four basic steps: Nutrition Assessment,
Nutrition Diagnosis, Nutrition Intervention and
Nutrition Monitoring and Evaluation (34).
Nutrition assessment is a systematic and
continual process of obtaining, verifying, and
interpreting data upon which the decisions about
the impact and cause of nutrition-related
problems are made. The process includes
review and analysis of medical, nutritional,
laboratory
data
and
food-medication
interactions;
obtaining
anthropometric
measurements;
and
reviewing
physical
examination results (assessment of visual signs
of malnutrition, oral status, chewing/swallowing
ability, and/or diminished ability to eat
independently, etc.).
with fortified foods at each meal and a 6 ounce
nutritional supplement at 2:00 PM and HS” (34).
A German study conducted by Hengstermann et
al. (35) concluded that the Mini Nutritional
Assessment, a validated nutrition assessment
tool, was “easy to use to determine the nutrition
status in multi-morbid geriatric patients with
pressure ulcers.” The American Dietetic
Association (ADA) Nutrition Risk Assessment is
commonly utilized in long-term care, and was
recently validated in a small study conducted by
ADA (36,37). Further research is planned to
complete the validation process.
Serum albumin levels have historically been
used widely in practice, however they are a poor
indicator of visceral protein status. This is due to
albumin’s long half-life (12 to 21 days) and
multiple factors which decrease albumin levels
even when protein intake is adequate (e.g.,
infection, acute stress, surgery, cortisone
excess, hydration status). Decreases in serum
albumin may reflect the presence of
inflammatory cytokine production or other
comorbidities rather than nutritional status (40).
Cytokine production may result in albumin being
pulled from the intravascular spaces into the
extravascular spaces and circulating back to the
liver until the inflammatory process is resolved.
Recent studies show the hepatic proteins
(albumin, transthyretin and transferrin) correlate
with the severity of an underlying disease rather
than nutritional status (41). Conversely,
dehydration may falsely elevate albumin levels.
Following the assessment, the registered
dietitian (RD) identifies and determines a
specific nutrition diagnosis or problem that the
dietetics professional is responsible for treating.
The intervention is specific to the nutrition
diagnosis or problem.
The monitoring and
evaluation steps determne the progress made
by the individual to meet the specific goals
established. An example of the nutrition
diagnosis for an individual with a pressure ulcer
is: “Inadequate food and fluid intake related to
less than 50% intake of meals as evidenced by
non-healing Stage IV pressure ulcer and five
pound weight loss in two weeks.” The nutrition
intervention is related to the specific nutrition
diagnosis. The client/individual and the other
members of the healthcare team would work
together
to
develop
appropriate
and
individualized interventions, and then monitor
and evalutate for needed changes to nutrition
interventions. In this case, an example of a
nutrition intervention is: “Provide a regular diet
©2009 NPUAP
Biochemical Data
Biochemical data analysis is one component of
the total nutrition assessment process. Although
laboratory tests may help clinicians evaluate
nutrition issues in patients at risk for a pressure
ulcer or for those who already have a pressure
ulcer, no laboratory test can specifically
determine an individual’s nutritional status.
Serum albumin, prealbumin and other lab values
may be useful to help establish overall
prognosis; however, they may not correlate well
with clinical observation of nutritional status
(38,39).
Due to its short half-life (2 to 3 days), prealbumin
(or transthyretin and thyroxine-binding albumin)
has historically been used by practitioners with
the assumption that it may be a better indicator
of the effectiveness of interventions used to
improve clinical condition (including nutrition
status). However, prealbumin is subject to the
same influences that make albumin problematic
when used as a nutritional indicator. Metabolic
stress and inflammation may decrease levels;
and converse to what practitioners may assume,
prealbumin levels may be maintained during
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The Role of Nutrition in Pressure Ulcer Prevention and Treatment:
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states of malnutrition (42). For these reasons, it
is not recommended as a marker for nutritional
status (41,43-49).
One study of critically ill patients receiving total
parenteral nutrition (TPN) failed to demonstrate
that an increase in the prealbumin level
indicated a better prognosis for this population
(45). However, monitoring of low levels of serum
hepatic proteins indicate that a person is very ill
and therefore at high risk for undernutrition,
PEM and unintended weight loss. In these
cases, the individual would benefit from
aggressive and frequent monitoring of weight
and oral intake and appropriateness of nutrition
interventions.
Current laboratory values are not always readily
available, and waiting for test results may further
delay nutritional intervention. Evaluation of lab
values is only one aspect of the nutritional
assessment process and should be considered
along with other factors such as daily food/fluid
intake, changes in weight status, diagnosis and
medications.
Nutritional Considerations in Pressure
Ulcer Treatment
Nutritional recommendations are primarily based
on expert opinion, best practice guidelines and
smaller studies. Each clinician must use expert
clinical judgment based on a thorough medical
and nutritional assessment to make appropriate
individualized
recommendations.
The
individualized care plan should focus on
improving and/or maintaining the patient’s
overall nutritional status, acceptance of nutrition
interventions, and clinical outcomes.
Macronutrients and Micronutrients
Related to Pressure Ulcer Treatment
Macronutrients
Energy
Energy, or kilocalories, are provided through the
macronutrients:
carbohydrates,
fats
and
proteins. Energy is essential for pressure ulcer
healing.
Providing
adequate
kilocalories
promotes anabolism, nitrogen and collagen
synthesis and healing (50). Increased calories
are needed to overcome accelerated loss of
©2009 NPUAP
energy and protein due to hypermetabolism
which occurs in malnourished patients (14)
Carbohydrate in the form of glucose is the major
fuel source for collagen synthesis, which is the
building block of tissue. Providing sufficient
carbohydrate as the primary fuel source is much
more efficient than synthesis of glucose from
protein and fat.
Provision of sufficient caloric requirements
should be based on achieving individualized
nutritional goals. Energy needs are currently
assessed using several methods. The methods
used for predictive formulas or energy needs
measurement must be defined for individual
populations (e.g., critically ill, obese). Recent
research indicates that the Harris-Benedict
equation is inaccurate for calculating energy
requirements (51). The Mifflin-St. Jeor Equation
may be more accurate and have a smaller
margin of error when used to calculate resting
metabolic rate for healthy obese individuals (52).
Measured energy requirements (i.e. indirect
calorimetry), if available, is a more accurate
measure of energy expenditure but cost may be
prohibitive in most settings.
The National
Academy of Sciences, Institute of Medicine, and
Food and Nutrition Board in partnership with
Health Canada (53) defined estimated energy
requirements needed to maintain energy
balance in a healthy individual.
The
requirements are defined by age, gender,
weight, height and activity; and form the basis
for determining baseline caloric requirements.
Calories may be adjusted upwards or
downwards based on individual nutritional
assessment. Individuals in a hypermetabolic
state have caloric requirements above the
baseline caloric requirements.
Caloric needs are ideally met by a healthy diet;
however some individuals are unable or
unwilling to consume an adequate diet. Overly
restricted diets may make food unpalatable and
unappealing and therefore reduce intake. The
ADA’s position statement indicates that quality
of life and nutritional status are enhanced by the
liberalization of the diet ordered by the physician
(54). For example, an individual may not find a
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The Role of Nutrition in Pressure Ulcer Prevention and Treatment:
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sodium restricted diet appealing and therefore
intake may be poor, leading to undernutrition
and slowing the pressure ulcer healing process.
The type and amount of food/fluid ingested daily
should be reviewed periodically to ensure the
individual actually ingests enough calories
based on estimated needs. It is also important to
examine the reasons for the intake being
decreased. Oral nutritional supplements,
enhanced foods, and food fortifiers can be used
to combat unintended weight loss and
undernutrition.
In a retrospective uncontrolled cohort study of
1524 residents in long-term care facilities, the
prescription of an oral supplement was a
predictor of pressure ulcer healing (16,17).
Desneves et al. conducted a randomized
controlled clinical trial (RCT) to measure
pressure ulcer healing using the Pressure Ulcer
Scale for Healing (PUSH) scores for three
different groups of subjects (55). Group A
received a standard hospital diet. Group B
received a standard diet plus two high calorie
supplements totaling 500 Kcalories, 18 grams of
protein, 72 mg of vitamin C and 7.5 mg of zinc.
Group C received a standard diet plus two high
calorie supplements which provided 500
Kcalories, 21 grams of protein, 9 grams of
additional arginine, 500 mg of vitamin C and 50
mg of zinc. Of the three groups, group C noted a
2.5 fold greater improvement in healing as
measured by a lower PUSH score. However,
this was a small three week intervention study of
only 16 subjects and pressure ulcers were not
described by stage. Therefore it is not possible
to determine the impact of the diet by stage of
pressure ulcer. A study conducted by Wilson
and colleagues indicated that individuals who
consumed oral nutritional supplements between
meals experienced better absorption of nutrients
with the least interference to meal intake (56).
Nutritional supplements include products that
supply nutrients such protein, calories, fat,
vitamins, minerals and/or amino acids.
Protein
Protein is the basis of the human body structure.
Proteins
are
uniquely
different
from
carbohydrates and fats (lipids) as only protein
©2009 NPUAP
contains nitrogen. Protein is responsible for the
synthesis of enzymes involved in pressure ulcer
healing, cell multiplication, and collagen and
connective tissue synthesis. All stages of
healing require adequate protein. Caloric
(energy) needs must be met first in order to
spare protein from being utilized as an energy
source.
Protein is essential to promote positive nitrogen
balance. Increased protein levels have been
linked to improved healing rates (57-61). Dietary
protein is especially important in the older adult
due to body composition changes that occur
with aging and reduced activity levels. These
changes may include sarcopenia and decreased
immune function, which can lead to impaired
wound healing and the inability to adequately
fight infection. Sarcopenia, normal age-related
loss of muscle, can be accelerated due to hypercatabolic disease states and production of
inflammatory cytokines which are liberated in
tissue injury. Recent studies indicate the basic
requirement for exogenous protein in older
adults is a minimum of 1.0 gram per kilogram
body weight, rather than 0.8 gram per kilogram
of body weight for healthy adults (62).
The recommended range of protein associated
with healing currently is between 1.2 to 1.5
grams per kilogram of body weight per day (63).
Past studies have indicated that protein levels
as high as 2.0 grams per kilogram body weight
may not increase protein synthesis and may
contribute to dehydration in the elderly (64).
Wolfe and Miller (65) noted that a protein level
above the recommended 0.8 per kilogram of
body weight for healthy adults is appropriate
under conditions such as wound healing.
Campbell, Trapp, Wolfe, et al. suggest a protein
allowance of at least 1.0 to 1.2 grams per
kilogram of body weight per day for healthy
elderly individuals (66). The Agency for Health
Care Policy and Research (AHCPR, which has
been renamed Agency for Healthcare Research
and Quality, or AHRQ) pressure ulcer treatment
guidelines recommend 1.25 to 1.5 grams per
kilogram of body weight per day for patients with
pressure ulcers (67). The European Pressure
Ulcer Advisory Panel (EPUAP) guideline
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controlled clinical trial in elderly nursing
home residents with pressure ulcers
reported that arginine supplementation
was well tolerated but did not enhance
mitogen-induced lymphocyte proliferation
or healing (69). In a small 3 week
interventional RCT, Desneves et al.
noted a reduction in PUSH scores for
individuals with pressure ulcers who
consumed high calorie supplements
containing arginine (55). Maximum safe
dosages of arginine supplementation in
humans have not been established.
Additional research is needed to
recommend the use of arginine alone or
combined with other nutrients for
pressure ulcer healing (70).
recommends 1.0 to 1.5 grams per kilogram of
body weight per day (50).
Some recent studies have focused on increasing
the amount of protein provided for wound
healing.
In one study, 89 nursing home
residents with Stage II, III and IV pressure ulcers
were randomized into a treatment group which
received standard care plus a concentrated,
fortified,
collagen
protein
hydrolysate
supplement three times a day (providing an
additional 45 grams protein per day), and a
control group which received standard care plus
a placebo three times a day. PUSH scores were
used to analyze wound healing. In the eight
week study period, those in the treatment group
had a fifty percent reduction in the PUSH scores
compared to those in the control group (58).
Additional studies are needed to determine
whether higher amounts of protein are safe and
effective in promoting pressure ulcer healing.
It is also important to note that nitrogen losses
may occur from exudating pressure ulcers,
possibly increasing protein needs. Clinical
judgment is required to determine the
appropriate level of protein for each individual,
based on the number of pressure ulcers, overall
nutritional status, comorbidities, and tolerance to
nutritional
interventions.
For
example,
individuals with chronic kidney disease may be
inappropriate candidates for high levels of
protein (68).
Amino Acids
Amino acids are the building blocks of protein.
Certain amino acids such as arginine and
glutamine become conditionally essential amino
acids during periods of severe stress such as
trauma, sepsis, and/or pressure ulcers.
Arginine
Arginine stimulates insulin secretion,
promotes the transport of amino acids
into tissue cells and supports the
formation of protein in the cells. Studies
related to wound healing appear to be
controversial and there is no definitive
research study specifically related to
arginine’s impact on pressure ulcer
healing in humans. A randomized
©2009 NPUAP
Glutamine
Glutamine’s role in pressure ulcer
healing may be its function as a fuel
source for fibroblasts and epithelial cells
needed for healing. The safe maximum
dose for glutamine supplementation has
been established as 0.57 grams per
kilogram of body weight per day (71).
Supplemental glutamine has not been
shown to improve wound healing (72).
More studies are needed to determine
glutamine’s impact on pressure ulcer
healing.
Fluids
Fluids serve as the solvent for vitamins,
minerals, glucose and other nutrients and the
transport medium for nutrients and waste
products though the body. Preliminary data from
Stotts and Harriet (73) indicate that fluid
administration may increase low tissue oxygen.
Tissue oxygenation is needed for proper
healing.
The RD calculates individual fluid requirements
and determines nutritional interventions. Various
formulas have been used to calculate adequate
daily fluid intake. One general formula utilizes 1
mL per kcalorie consumed (50) initially.
Practitioners must assess for tolerance and
reassess as condition changes.
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Health care practitioners should monitor
individuals’ hydration status, checking for signs
and symptoms of dehydration such as: changes
in weight, skin turgor, urine output, elevated
serum sodium or calculated serum osmolality
(74).
Individuals consuming high levels of protein may
require additional fluid. Elevated temperature,
vomiting, profuse sweating, diarrhea and heavily
draining wounds contribute to fluid loss which
must be replaced (74).
patients with pressure ulcers who were
randomized to receive 10 mg or 500 mg of
vitamin C twice daily. The study did not result in
improved healing in either of the two groups
(79). The inclusion of fruits and vegetables such
as citrus fruits in the diet can achieve the
desired recommended daily amount. However,
vitamin C at physiological doses should be
considered
when
dietary
deficiency
is
diagnosed.
In generally healthy individuals who are
adequately hydrated, food accounts for any
where from 19 to 28% of total fluid intake (75).
Total fluid needs include the water content of the
food consumed (75). Nutritional supplements
and enteral feedings are generally 75% water.
For specific amount of free fluids refer to the
individual product nutrition labeling.
Zinc is a mineral that functions as an antioxidant
and is associated with collagen formation,
synthesis of protein, DNA and RNA, and cell
proliferation. Inflammatory cells, epithelial cells
and fibroblasts are proliferating cells (80). Zinc is
transported through the body primarily by
albumin, therefore, zinc absorption declines
when plasma albumin declines, such as in PEM,
trauma, sepsis or infection (81).
Micronutrients
The Institute of Medicine (IOM), National
Academy of Sciences (NAS) Dietary Reference
Intakes indicate the level of each micronutrient
needed at each stage of life for healthy
individuals (53,76). Most nutrient needs can be
met through a healthy diet. However, individuals
with pressure ulcers may not be consuming an
adequate diet to meet established nutritional
reference standards.
Micronutrients that are “hypothesized” to be
related to pressure ulcer healing include vitamin
C, zinc and copper.
Ascorbic Acid
Ascorbic acid (vitamin C), a water soluble
vitamin, is a cofactor with iron during the
hydroxylation of proline and lysine in the
production of collagen. Thus ascorbic acid is
important for tissue repair and regeneration (77).
Deficiency can be associated with impaired
fibroblastic function and decreased collagen
synthesis, which can result in delayed healing
and capillary fragility. Ascorbic acid deficiency is
also associated with impaired immune function
which can decrease the ability to fight infection
(77). However, mega doses of vitamin C have
not been shown to accelerate wound healing
(78). One blinded, multicenter trial included 88
©2009 NPUAP
Zinc and Copper
Deficiency of zinc may be the result of wounds
with increased drainage, poor dietary intake over
a long period of time, or excessive
gastrointestinal losses. Zinc deficiency may
cause loss of appetite, abnormal taste, impaired
immune function and impaired wound healing.
Good sources of zinc include high protein foods
such as meat, liver, and shellfish.
No research has demonstrated an effect of zinc
supplementation on improved pressure ulcer
healing. When clinical signs of zinc deficiency
are present, zinc should be supplemented at no
more than 40 mg of elemental zinc per day
which is the Daily Reference Intakes (DRI)
upper limit (82). Zinc supplementation should be
stopped once the deficiency is corrected. Highdose zinc supplementation (above 40 mg per
day) is not recommended (76) because it can
adversely affect copper status possibly resulting
in anemia. High serum zinc levels may inhibit
healing, impair phagocytosis, interfere with
copper metabolism, and induce a copper
deficiency since both minerals compete for
binding sites on the albumin molecule (15,83,
84). Copper deficiency may be harmful as
copper is essential for collagen cross-linking.
Nutrition White Paper
8
The Role of Nutrition in Pressure Ulcer Prevention and Treatment:
National Pressure Ulcer Advisory Panel White Paper
To determine if additional supplementation is
necessary and before recommending additional
supplementation, practitioners should review
any
comprehensive
vitamin/mineral
supplements, enteral formulas, oral nutritional
supplements or fortified foods which contain
additional micronutrients.
Current Recommendations for Medical
Nutrition Therapy for Pressure Ulcer
Treatment
The following recommendations are taken from
the NPUAP-EPUAP Pressure Ulcer Treatment
Guideline, published in 2009. The Treatment
Guideline was developed following a systematic,
comprehensive review of the peer-reviewed,
published research on pressure ulcer treatment
from 1998 through January 2008. Supplemental
searches were conducted on related nutrition
issues. Evidence tables from previous guidelines
were reviewed to identify relevant studies
published prior to 1998. All studies meeting
inclusion criteria were reviewed for quality,
summarized in evidence tables and classified
according to their level of evidence using a
schema developed by Sackett (85).
Sackett Level of Evidence Rating System
for Individual Studies
Level
I
II
III
IV
V
Large randomized trial with clear-cut
results (and low risk of error)
Small randomized trial with uncertain
results (and moderate to high risk of
error)
Non randomized trial with concurrent or
contemporaneous controls
Non randomized trial with historical
controls
Case Series with no controls. Specify
number of subjects.
Adapted from Sackett DL/ Evidence based
medicine. What it is and what it isn't. Br Med J
1996;312:71-72.
B – Recommendation supported by direct
scientific evidence from properly designed and
implemented clinical series on pressure ulcers in
humans providing statistical results that
consistently support the recommendation
(Sackett Level II, III, IV, V studies).
C – The recommendation is supported by expert
opinion or indirect evidence (e.g. studies in
animal models and/or other types of chronic
wounds).
A complete description of the NPUAP-EPUAP
guideline development methodology has been
previously published (86).
Additional research is needed to determine the
effects of various medical nutrition therapy
(MNT) interventions on pressure ulcer healing.
The goals of MNT must also be based on the
individual’s prognosis and goals of treatment.
For
some,
aggressive
intervention
is
appropriate. However, for others, such as those
at end of life, the goal may simply be to maintain
comfort to the extent possible based on the
patient’s wishes.
For individuals who have a pressure ulcer,
the NPUAP-EPUAP guidelines are:
All individuals should have a nutritional
assessment upon admission and with each
condition change. This is particularly true
for individuals with pressure ulcers.
1. Screen and assess nutritional status for
each individual with a pressure ulcer at
admission and with each condition
change and/or when progress toward
pressure ulcer closure is not observed.
(Strength of Evidence = C.)
Strength of Evidence Supporting Each
Recommendation
Next the cumulative strength of evidence
supporting each recommendation was rated
according to the following criteria:
©2009 NPUAP
A – Recommendation supported by direct
scientific evidence from properly designed and
implemented controlled trials on pressure ulcer
in humans providing statistical results that
consistently support the recommendation
(Sackett Level I studies).
1.1.
Nutrition White Paper
Refer all individuals with a
pressure ulcer to the dietitian for
9
The Role of Nutrition in Pressure Ulcer Prevention and Treatment:
National Pressure Ulcer Advisory Panel White Paper
early assessment and intervention
of nutritional problems. (Strength
of Evidence = C.)
1.2.
1.3.
1.4.
Assess weight status for each
individual to determine weight
history and significant weight loss
from usual body weight (> 5%
change in 30 days or > 10% in 180
days). (Strength of Evidence = C.)
Assess
ability
to
independently.
(Strength
Evidence = C.)
2.4.
3. Provide adequate protein for positive
nitrogen balance for an individual with a
pressure ulcer. (Strength of Evidence =
B.)
eat
of
3.1.
Assess adequacy of total nutrient
intake
(food,
fluid,
oral
supplements,
enteral/parenteral
feedings). (Strength of Evidence =
C.)
Offer 1.25 - 1.5 grams protein/kg
body weight for an individual with
a pressure ulcer when compatible
with goals of care, and reassess
as condition changes. (Strength of
Evidence = C.)
3.2.
Assess renal function to ensure
high levels of protein are
appropriate for the individual.
(Strength of Evidence = C.)
2. Provide sufficient calories. (Strength of
Evidence = B.)
2.1.
Consider
nutritional
support
(enteral or parenteral nutrition)
when oral intake is inadequate.
This must be consistent with
individual goals. (Strength of
Evidence = C.)
Provide 30-35 Kcalories/kg body
weight for individuals under stress
with a pressure ulcer.
Adjust
formula based on weight loss,
weight gain or level of obesity.
Individuals who are underweight
or who have had significant
unintentional weight loss may
need additional Kcalories to cease
weight loss and/or regain lost
weight. (Strength of Evidence = C.)
2.2.
Revise and modify (liberalize)
dietary
restrictions
when
limitations result in decreased
food and fluid intake. This is to be
done by a dietitian or medical
professional.
(Strength
of
Evidence = C.)
2.3.
Provide enhanced foods and/or
oral supplements between meals if
needed. (Strength of Evidence =
B.)
©2009 NPUAP
4. Provide and encourage adequate daily
fluid intake for hydration. (Strength of
Evidence = C.)
4.1.
Monitor individuals for signs and
symptoms
of
dehydration:
changes in weight, skin turgor,
urine output, elevated serum
sodium or calculated serum
osmolality. (Strength of Evidence
= C.)
4.2.
Provide
additional
fluid
for
individuals
with
dehydration,
elevated
temperature, vomiting,
profuse sweating, diarrhea or
heavily draining wounds. (Strength
of Evidence = C.)
5. Provide adequate vitamins and minerals.
(Strength of Evidence = B.)
5.1.
Nutrition White Paper
Encourage consumption of a
balanced diet which includes good
sources of vitamins and minerals.
(Strength of Evidence = B.)
10
The Role of Nutrition in Pressure Ulcer Prevention and Treatment:
National Pressure Ulcer Advisory Panel White Paper
5.2.
Offer
vitamin
and
mineral
supplements when dietary intake
is poor or deficiencies are
confirmed or suspected. (Strength
of Evidence = B.)
Research Needs
Undernutrition is associated with increased
morbidity and mortality. Early identification and
treatment of nutritional problems is critical.
There were no studies specifically addressing
the obese individual with pressure ulcers.
Additional research is also needed for pediatric
patients and neonates. Appetite stimulants and
anabolic steroids may have a role in improving
body weight; however, more research is needed
to determine effectiveness in promoting
pressure ulcer healing.
Research is needed to better define appropriate
caloric range for obese individuals (those with
BMI >30) with pressure ulcers. Although weight
loss is usually recommended for obese
individuals, weight loss efforts may need to be
modified or postponed temporarily to provide
sufficient nutrients for pressure ulcer healing.
It is essential to meet minimal recommended
dietary intake (RDI). Protein levels for patients
with wounds should be 1.25-1.5 grams of
protein. Randomized clinical trials indicate
increased protein levels promote pressure ulcer
healing.
The research to date does not
demonstrate the effectiveness of branched chain
or individual amino acids, such as arginine and
glutamine, in the treatment of pressure ulcers.
Further study is needed.
Recommendations are based on good clinical
practice as the evidence specific to fluid
requirements and pressure ulcers is lacking.
There is no research to justify administration of
vitamin/mineral supplements that are above the
US RDI or comparable European or international
standards.
Ethical and Clinical Implications for
Practice
Clinicians need evidence-based research results
to develop appropriate clinical guidelines for
©2009 NPUAP
nutrition assessment and intervention. Nutrition
and hydration can have a positive impact on the
quality of life. Poor health outcomes may be
associated with even small amounts of
unintended weight loss. Early nutrition
interventions can help to prevent and/or delay
undernutrition, PEM and hydration deficits and
their impact on risk of pressure ulcer
development and delayed healing. Refer the
patient to the RD as soon as risk is identified or
upon identification of a pressure ulcer. If
medically possible, early aggressive nutrition
interventions should be implemented to prevent
or correct nutrition deficits. For individuals at the
end of life, however, nutrition interventions must
be weighed against the burdens versus benefits
and patient preferences.
If oral intake is inadequate, the registered
dietitian may recommend consideration of
enteral or parenteral nutrition consistent with the
patient’s wishes. Enteral (tube) feeding is the
preferred route if the gastrointestinal tract (GI) is
functioning. The risks and benefits of nutrition
support should be discussed with the individual
and caregivers early on, and should reflect the
individual’s preferences and goals for care.
Studies that have reviewed enteral nutrition for
improved outcomes for pressure ulcers have
been disappointing (60,87,88). If enteral feeding
is provided, health practitioners should routinely
monitor feedings to ensure individuals are
actually receiving the amount of tube feeding
solution prescribed.
Acknowledgements
Becky Dorner, RD, LD, is President, Becky
Dorner & Associates, Inc, and Nutrition
Consulting Services, Akron, Ohio; Mary Ellen
Posthauer, RD, CD, is a Consultant Dietitian and
Chief Executive Officer of MEP Healthcare
Services, Evansville, Indiana; David Thomas,
MD, CMD, FACP, is Professor of Medicine,
Saint Louis University, Saint Louis, Missouri.
The authors thank the National Pressure Ulcer
Advisory Panel board for its approval of this
document on December 22, 2008: Joyce Black,
PhD, RN; Mona M. Baharestani, PhD, ANP,
CWON, CWS; Evan Call, MS; Janet Cuddigan,
PhD, RN, CWCN, CCCN; Teresa Conner-Kerr,
Nutrition White Paper
11
The Role of Nutrition in Pressure Ulcer Prevention and Treatment:
National Pressure Ulcer Advisory Panel White Paper
PhD, PT, CWS, CLT; Becky Dorner, RD, LD;
Laura Edsberg, PhD; Aimee´ Garcia, MD; Susan
Garber, MA, OTR, FAOTA, FACRM; Diane
Langemo, PhD, RN, FAAN; Laurie McNichol,
MSN, RN, GNP, CWOCN; Barbara Pieper, PhD,
RN, CS, CWOCN, FAAN; Catherine Ratliff, PhD,
APRN-BC, CWOCN; Steven Reger, PhD, CP;
and Greg Schultz, PhD.
10.
The authors also thank the reviewers of the
document: Diane Langemo, PhD, RN, FAAN;
Janet Cuddigan, PhD, RN, CWCN, CCCN;
Steven Black, MD; and Lynn Moore, RD, LD.
References
1.
2.
3.
4.
5.
6.
7.
8.
9.
Lyder C, Yu C, Stevenson D, Mangat R, EmpleoFrazier O, Emerling J, McKay J. Validating the
Braden Scale for the prediction of pressure ulcer
risk in blacks and Latino/Hispanic elders: a pilot
study. Ostomy Wound Manage. 1998;44(suppl
3A):42S-49S.
Strategies for Preventing Pressure Ulcers, Joint
Commission Perspectives on Patient Safety,
Volume 8, Number 1, January 2008, pp.5-7(3).
http://www.jcrinc.com/Pressure-Ulcers-stage-IIIIV-decubitis-ulcers/. Accessed March 23, 2009.
Cuddigan J, Ayello EA, Sussman C, Baranoski
S, eds. Pressure Ulcers in America: Prevalence,
Incidence, and Implications for the Future.
Reston, VA: National Pressure Ulcer Advisory
Panel; 2001.
Lyder CH. Pressure ulcer prevention and
management. JAMA. 2003;289:223-226.
Russo CA, Steiner C and Spector W.
Hospitalizations Related to Pressure Ulcers
among Adults 18 Years and Older, 2006.
Healthcare Cost Utilization Project. December
2008.
Available
at:
http://www.hcupus.ahrq.gov/reports/statbriefs/sb64.jsp.
Accessed December 22, 2008.
Berlowitz DR, Brandeis GH, Anderson J, Du W,
Brand H. Effect of pressure ulcers on the survival
of long-term care residents. J Gerontol A Biol Sci
Med Sci. 1997;52:M106-M110.
Thomas DR, Goode PS, Tarquine PH, Allman
RM. Hospital-acquired pressure ulcers and risk
of death. J Am Geriatr Soc. 1996;44:1435-1440.
Beckrich K, Aronovitch SA. Hospital-acquired
pressure ulcers: a comparison of costs in
medical vs. surgical patients. Nurs Econ.
1999;17:263-271.
Centers for Medicare & Medicaid Services.
Proposed Fiscal Year 2009 Payment, Policy
Changes for Inpatient Stays in General Acute
©2009 NPUAP
11.
12.
13.
14.
15.
16.
17.
18.
Care
Hospitals.
Available
at
http://www.cms.hhs.gov/apps/media/press/factsh
eet.asp?Counter=3045&intNumPerPage=10&ch
eckDate=&checkKey=&srchType=1&numDays=3
500&srchOpt=0&srchData=&keywordType=All&c
hkNewsType=6&intPage=&showAll=&pYear=&y
ear=&desc=&cboOrder=date.
Accessed
December 3, 2008.
Centers for Medicare & Medicaid Services.
Medicare Program; Proposed Changes to the
Hospital Inpatient Prospective Payment Systems
and Fiscal Year 2009 Rates; Proposed Changes
to Disclosure of Physician Ownership in
Hospitals and Physician Self-Referral Rules;
Proposed Collection of Information Regarding
Financial Relationships Between Hospitals and
Physicians: Proposed Rule. Federal Register.
2008:73(84):23550.
Available
at
http://edocket.access.gpo.gov/2008/pdf/081135.pdf. Accessed December 3, 2008.
Graves N, Birrell F, Whitby M. Effect of pressure
ulcers on length of hospital stay. Infect Control
Hosp Epidemiol. 2005;26:293-297.
Voss AC, Bender SA, Ferguson ML, Sauer AC,
Bennett RG, Hahn PW. Long-term care liability
for pressure ulcers. J Am Geriatr Soc.
2005;53:1587-1592.
Hahn P. Report and Results of Updated
Research on Nursing Home Liability for Pressure
Ulcers. Columbus, Ohio: Buckingham, Doolittle &
Burroughs, LLP; 2002.
Pinchcofsky-Devin GD, Kaminski MV Jr.
Correlation of pressure sores and nutritional
status. J Am Geriatr Soc. 1986;34:435-440.
Thomas DR. The role of nutrition in prevention
and healing of pressure ulcers. Clin Geriatr Med.
1997;13:497-511.
Horn SD, Bender SA, Ferguson ML, Smout RJ,
Bergstrom N, Taler G, Cook AS, Sharkey SS,
Voss AC. The National Pressure Ulcer LongTerm Care Study: pressure ulcer development in
long-term care residents. J Am Geriatr Soc.
2004;52:359-367.
Bergstrom N, Horn SD, Smout RJ, Bender SA,
Ferguson ML, Taler G, et al. (2005). The
National Pressure Ulcer Long-Term Care Study:
Outcomes of pressure ulcer treatments in longterm care. Journal of the American Geriatrics
Society, 53:1721-1729, 2005.
Centers for Medicare & Medicaid Services.
State Operations Manual, Guidance to Surveyors
for Long Term Care Facilities, Appendix PP.
http:www.cms.hhs.gov/GuidanceforLawsAndReg
ulations/12_NHs.asp.Revision 26, September 1,
2008. Accessed September 30, 2008.
Nutrition White Paper
12
The Role of Nutrition in Pressure Ulcer Prevention and Treatment:
National Pressure Ulcer Advisory Panel White Paper
19. Gilmore S A, Robinson G, Posthauer M E, &
Raymond
J.
(1995).
Clinical
indicators
associated with unintentional weight loss and
pressure ulcers in elderly residents of nursing
facilities. J Am Diet Assoc, 95(9), 984-992.
20. Horn SD, Bender SA, Bergstrom N, Cook AS,
Ferguson ML, Rimmasch HL, Sharkey SS,
Smout RJ, Taler GA, Voss AC. Description of the
National Pressure Ulcer Long-Term Care Study.
J Am Geriatr Soc. 2002;50:1816-1825.
21. Thomas, D.R. Unintended weight loss in older
adults. Aging Health 2008;4(2),191-200.
22. Murden R A, & Ainslie N K. (1994). Recent
weight loss is related to short-term mortality in
nursing homes. Journal Of General Internal
Medicine: Official Journal Of The Society For
Research And Education In Primary Care
Internal Medicine, 9(11), 648-650.
23. Ryan C, Bryant E, Eleazer P, Rhodes A, & Guest
K. (1995). Unintentional weight loss in long-term
care: predictor of mortality in the elderly.
Southern Medical Journal, 88(7), 721-724.
24. Sullivan D H, Johnson L E, Bopp M M, &
Roberson P K. (2004). Prognostic significance of
monthly weight fluctuations among older nursing
home residents. The Journals of Gerontology.
Series A, Biological Sciences and Medical
Sciences, 59(6), M633-639.
25. Thomas D R. (2007). Loss of skeletal muscle
mass in aging: examining the relationship of
starvation, sarcopenia and cachexia. Clinical
Nutrition, 26(4), 389-399.
26. ASPEN Board of Directors and the Clinical
Guidelines Task Force. Guidelines for the use of
parenteral and enteral nutrition in adult and
pediatric patients. J Parenter Enteral Nutr.
2002;26:22SA-24SA.
27. Bergstrom N, Braden B. A prospective study of
pressure ulcer sore risk among institutionalized
elderly, Journal of the American Geriatric Society
40(8): 747-58. August, 1992.
28. Evans WJ, Morley JE, Argiles J, Bales C,
Baracos V, Guttridge D, Jatoi A, Kalantar-Zadeh
K, Lochs H, Mantovani G, Marks D, Mitch WE,
Muscaritoli M, Najand A, Ponikowski P, Rossi
Fanelli F, Schambelan M, Schols A, Schuster M,
Thomas D, Wolfe R, Anker SD. Cachexia: a new
definition. Clinical Nutrition. 27(6):793-9, 2008.
29. MacIntosh C, Morley JE, Chapman IM. The
anorexia of aging. Nutrition. 2000;16:983-995.
30. Langkamp-Henken B, Hudgens J, Stechmiller J
K, & Herrlinger-Garcia K A. (2005). Mini
nutritional assessment and screening scores are
associated with nutritional indicators in elderly
people with pressure ulcers. Journal Of The
©2009 NPUAP
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
American Dietetic Association, 105(10 (Print)),
1590-1596.
Hudgens, J., Langkamp-Henken, B., Stechmiller,
J. K., Herrlinger-Garcia, K. A., & Nieves, C., Jr.
(2004). Immune function is impaired with a mini
nutritional assessment score indicative of
malnutrition in nursing home elders with pressure
ulcers. JPEN. Journal Of Parenteral And Enteral
Nutrition, 28(6), 416-422.
BAPEN (British Association of Parenteral and
Enteral Nutrition) Malnutrition Advisory Group,
The MUST Report, Nutritional screening of
adults: a multidisciplinary responsibility. (2008).
Journal.
Retrieved
from
http://www.bapen.org.uk/must_tool.html.
Braden B. The Braden Scale for Pressure Ulcer
Prediction.
Available
at:
http://www.bradenscale.com/braden.PDF.
Accessed January 9, 2009.
American Dietetic Association. International
Dietetics and Nutrition Terminology (IDNT)
Reference Manual: Standardized Language for
the Nutrition Care Process. The American
Dietetic Association, Chicago, IL. Second
Edition, 2009.
Hengstermann S, Fischer A, SteinhagenThiessen E, Schulz RJ. Nutrition status and
pressure ulcer: what we need for nutrition
screening. JPEN J Parenter Enteral Nutr.
2007;31:288-294.
Beto J. Long-Term Care Nutrition Risk
Assessment Study. Consultant Dietitians in
Health Care Facilities, a dietetic practice group of
the American Dietetic Association. Chicago, IL.
2007.
Gallagher FA, Leif BJ, Niedert K, Robinson G.
Nutrition Risk Assessment. Chicago, Ill:
American Dietetic Association; 1999.
Covinsky KE, Covinsky MH, Palmer RM, Sehgal
AR. Serum albumin concentration and clinical
assessments of nutritional status in hospitalized
older people: different sides of different coins? J
Am Geriatr Soc. 2002;50:631-637.
Ferguson RP, O’Connor P ,Crabtree B,
Batchelor A, Mitchell J, Coppola D. Serum
albumin and prealbumin as predictors of
hospitalized elderly nursing home residents. J
Am Geriatr Soc.1993;41:545-549.
Friedman FJ, Campbell AJ, Caradoc-Davies TH.
Hypoalbuminemia in the elderly is due to disease
not malnutrition. Clinical Experimental Gerontol.
1985;7:191-203.
Myron Johnson A, Merlini G, Sheldon J, &
Ichihara K. (2007). Clinical indications for plasma
protein assays: transthyretin (prealbumin) in
Nutrition White Paper
13
The Role of Nutrition in Pressure Ulcer Prevention and Treatment:
National Pressure Ulcer Advisory Panel White Paper
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
inflammation and malnutrition. Clinical Chemistry
and Laboratory Medicine: CCLM / FESCC, 45(3),
419-426.
Mahan LK, Escott-Stump S, eds. Krauses’s
Food, Nutrition, and Diet Therapy. St Louis, MO:
WB Saunders (Elsevier); 2008.
Shenkin A. Serum prealbumin: Is it a marker of
nutritional status or of risk of malnutrition. Clin
Chem.
2006
Dec;52(12):2281-5;
PMID:
17068165. Clinical Chemistry. 52(12):2177-9,
2006 Dec.
Lim SH, Lee JS, Chae SH, Ahn BS, Chang
DJ, Shin CS. Prealbumin is not sensitive
indicator of nutrition and prognosis in critical ill
patients. Yonsei Medical Journal. 46(1):21-6,
2005 Feb 28.
Robinson MK. Trujillo EB. Mogensen KM.
Rounds J. McManus K. Jacobs DO. Improving
nutritional screening of hospitalized patients: the
role of prealbumin. J Parenter Enteral Nutr. 2004
Jul-Aug;28(4):281.
Fuhrman MP, Charney P, Mueller CM. Hepatic
proteins and nutrition assessment. Journal of the
American Dietetic Association. 104(8):1258-64,
2004 Aug.
Bachrach-Lindstrom M, Unosson M, Ek AC,
Arnqvist HJ. Assessment of nutritional status
using biochemical and anthropometric variables
in a nutritional intervention study of women with
hip fracture. Clinical Nutrition. 20(3):217-23,
2001 Jun.
Steinman TI. Serum albumin: its significance in
patients with ESRD. Seminars in Dialysis.
13(6):404-8, 2000
Nov-Dec.Ronchetti
IP,
Quaglino D Jr, Bergaminni G. Ascorbic acid and
connective
tissue.
Subcell
Biochem.
1996;25:249-264.
Dutton J, Campbell H, Tanner J, Richards N.
Pre-dialysis serum albumin is a poor indicator of
nutritional status in stable chronic hemodialysis
patients. Edtna-Erca Journal. 25(1):36-7, 1999
Jan-Mar.
Clark M, Schols J , Benati G, Jackson P, Engfer
M, Langer G, et al. (2004). Pressure ulcers and
nutrition: a new European guideline. Journal of
Wound Care, 13(7), 267-272.
American Dietetic Association Evidence Analysis
Library, 2008 ADA Evidence Analysis Library.
(2008).
Accessed
06/30/08,
from
http://www.adaevidencelibrary.com/topic.cfm?for
mat_tables=0&cat=3016
Frankenfield D, Roth-Yousey L. & Compher C.
(2005). Comparison of predictive equations for
resting metabolic rate in healthy nonobese and
©2009 NPUAP
53.
54.
55.
56.
57.
58.
59.
60.
61.
62.
63.
64.
obese adults: a systematic review. Journal of the
American Dietetic Association, 105(5), 775-789.
Institute of Medicine. National Academy of
Sciences (NAS): Dietary Reference Intakes for
Energy, Carbohydrate, Fiber, Fat, Fatty Acids,
Cholesterol,
Protein
and
Amino
Acids.
Washington, DC, 2005.
Position of the American Dietetic Association:
Liberalization of the diet prescription improves
quality of life for older adults in long-term care.
(2005). Journal of the American Dietetic
Association, 105(12), 1955-1965.
Desneves K J, Todorovic B E, Cassar A, &
Crowe
T
C.
(2005).
Treatment
with
supplementary arginine, vitamin C and zinc in
patients with pressure ulcers: a randomised
controlled trial. Clinical Nutrition (Edinburgh,
Scotland), 24(6 (Print)), 979-987.
Wilson M-M G, Purushothaman R, & Morley J E.
(2002). Effect of liquid dietary supplements on
energy intake in the elderly. The American
Journal Of Clinical Nutrition, 75(5), 944-947.
Hartgrink H H, Wille J, Konig P, Hermans J, &
Breslau P J. (1998). Pressure sores and tube
feeding in patients with a fracture of the hip: a
randomized clinical trial. Clinical nutrition
(Edinburgh, Scotland), 17(6), 287.
Lee S K, Posthauer M E, Dorner B., Redovian V,
& Maloney M J. (2006). Pressure ulcer healing
with a concentrated, fortified, collagen protein
hydrolysate supplement: a randomized controlled
trial. Advances In Skin & Wound Care, 19(2), 9296.
Pompeo M. (2007). Misconceptions about
protein requirements for wound healing: results
of a prospective study. Ostomy/Wound
Management, 53(8), 30. (Level V)
Chernoff RS, Milton K, Lipschitz DA. (1990). The
effect of a very high protein liquid formula on
decubitus ulcer healing in long-term tube-fed
institutionalized patients [abstract]. Journal of the
American Dietetic Association, 90(9), A-130.
Breslow RA, Bergstrom N. Nutritional prediction
of pressure sores. J Am Diet Assoc.
1994;94:1301-1306.
Chernoff R. Protein and older adults. J Am Coll
Nutr. 2004;23(suppl 6):627S-630S.
Yarkony GM. Pressure ulcers: A review. Arch
Phys Med Rehabil. 1994:75:908-917.
Long CL, Nelson KM, Akin JM Jr, Geiger JW,
Merrick HW, Blakemore WS. A physiologic basis
for the provision of fuel mixtures in normal and
stressed patients. J Trauma. 1990;30:10771086.
Nutrition White Paper
14
The Role of Nutrition in Pressure Ulcer Prevention and Treatment:
National Pressure Ulcer Advisory Panel White Paper
65. Wolfe R R, & Miller S L. (2008). The
recommended dietary allowance of protein: a
misunderstood concept. JAMA: The Journal Of
The American Medical Association, 299(24),
2891-2893.
66. Campbell WW, Trappe TA, Wolfe RR, & Evans
WJ. (2001). The recommended dietary
allowance for protein may not be adequate for
older people to maintain skeletal muscle. The
Journals of Gerontology. Series A, Biological
Sciences and Medical Sciences, 56(6), M373380.
67. Bergstrom N, Bennett MA, Carlson CE. (1994).
Treatment of Pressure Ulcers. Clinical Practice
Guideline, No. 15. Rockville, MD: Department of
Health and Human Services, Public Health
Service, Agency for Health Care Policy and
Research.
68. Clinical practice guidelines for nutrition in chronic
renal
failure.
K/DOQI,
National
Kidney
Foundation. (2000). American Journal of Kidney
Diseases: The Official Journal of the National
Kidney Foundation, 35(6 Suppl 2), S1-140.
69. Langkamp-Henken B, Herrlinger-Garcia K A,
Stechmiller J K, Nickerson Troy J A, Lewis B, &
Moffatt L. (2000). Arginine supplementation is
well tolerated but does not enhance mitogeninduced lymphocyte proliferation in elderly
nursing home residents with pressure ulcers. J
Parenter Enteral Nutr, 24(5), 280-287.
70. Langer, G; Schloemer, G; Knerr, A; Kuss, O;
Behrens, J. Nutritional interventions for
preventing and treating pressure ulcers. The
Cochrane Database of Systematic Reviews
Volume (1), 2007.
71. Ziegler TR, Benfell K, Smith RJ, Young LS,
Brown E, Ferrari-Baliviera E, Lowe DK, Wilmore
DW. Safety and metabolic effects of L-glutamine
administration in humans. JPEN J Parenter
Enteral Nutr. 1990;14(suppl 4):137S-146S.
72. McCauly R, Platell C, Hall J, McCulloch R.
Effects of glutamine infusion on colonic
anastamotic strength in the rat. JPEN J Parenter
Enteral Nutr. 1991;15:437-439.
73. Stotts N A, Hopf H. The Link Between Tissue
Oxygen and Hydration in Nursing Home
Residents With Pressure Ulcers: Preliminary
Data. Journal of Wound, Ostomy & Continence
Nursing. 30(4):184-190, July 2003.
74. Thomas D R, Cote T R, Lawhorne L, Levenson S
A, Rubenstein L Z, Smith D.A, et al. (2008).
Understanding clinical dehydration and its
treatment. Journal of The American Medical
Directors Association, 9(5), 292-301.
©2009 NPUAP
75. Institute of Medicine. National Academy of
Sciences (NAS): Dietary Reference Intakes for
Water, Potassium, Sodium, Chloride, and
Sulfate. Washington, DC, 2004. Available at:
http://www.iom.edu/?id=54343.
Accessed
December 22, 2008.
76. Institute of Medicine. National Academy of
Sciences (NAS): Dietary Reference Intakes: the
essential guide to nutrient requirements.
Washington, DC, 2006.
77. Ronchetti IP, Quaglino D, Bergamini G. Ascorbic
Acid and Connective Tissue. Subcellular
Biochemistry, Volume 25: Ascorbic Acid:
Biochemistry and Biomedical Cell Biology.
Plenum Press, New York, 1996.
78. Vilter RW. Nutritional aspects of ascorbic acid:
uses and abuses. West J Med 1980;133:485492.
79. ter Riet G, Kessels A G, & Knipschild P G.
(1995). Randomized clinical trial of ascorbic acid
in the treatment of pressure ulcers. J Clin
Epidemiol, 48(12), 1453-1460.
80. Stephens P and Thomas D. The Cellular
Proliferate Phase of the Wound Repair Process,
Journal of Wound Care 11:253-61, July 2002.
81. Cataldo CB, DeBruyne LK, Whitney EN. Nutrition
and Diet Therapy, Principles and Practice.
Belmonth, CA: Wadsworth; 2003.
82. Lowen D. Wound healing. In: Matarese
LE,Gottschlich MM,eds. Contemporary Nutrition
Support Practice: A Clinical Guide. Philadephia.
Pa: WB Saunders; 1998: 583-589.)
83. Reed BR, Clark RA. Cutaneous tissue repair:
practical implications of current knowledge. II. J
Amer Acad Dermatol. 1985;13:919-941.
84. Goode HF, Burns E, Walker BE. Vitamin C
depletion and pressure sores in elderly patients
with femoral neck fracture. BMJ. 1992;305:925927.
85. Sackett DL. Evidence based medicine. What it is
and what it isn't. Br Med J 1996;312:71-72.
86. Vanderwee K, Clark M, Dealey C, Defloor T, et
al. Development of clinical practice guideline on
pressure ulcers. EWMA Journal 2007;7(3)44-46.
87. Henderson C T, Trumbore L S, Mobarhan S,
Benya R, & Miles T P. (1992). Prolonged tube
feeding in long-term care: nutritional status and
clinical outcomes. Journal of the American
College of Nutrition, 11(3), 309-325.
88. Mitchell S L, Kiely D K, & Lipsitz L A. (1997). The
risk factors and impact on survival of feeding
tube placement in nursing home residents with
severe cognitive impairment. Archives of Internal
Medicine, 157(3), 327-332.
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